DOI: 10.1002/prot.340050406. The structure of aconitase

10.1002/prot.340050406

Crossref journal-article

Wiley

Proteins: Structure, Function, and Bioinformatics (311)

Abstract

AbstractThe crystal structure of the 80,000 Da FeS enzyme aconitase has been solved and refined at 2.1 Å resolution. The protein contains four domains; the first three from the N‐terminus are closely associated around the [3Fe–4S] cluster with all three cysteine ligands to the cluster being provided by the third domain. Associationof the larger C‐terminal domain with the first three domains createsan extensive cleft leading to the FeS cluster. Residues from all four domains contribute to the active site region, which is defined by the FeS cluster and a bound SOion. This region of the structure contains 4 Arg, 3 His, 3 Ser, 2 Asp, 1 Glu, 3 Asn, and 1 Gln residues, as well asseveral bound water molecules. Three of these side chains reside on a threeturn 310 helix in the first domain. The SOion is bound 9.3 Å from the center of the [3Fe–4S] cluster by the side chains of 2 Arg and 1 Gln rsidues. Each of 3 His side chains in the putative active site is paired with Asp or Glu side chains.

Bibliography

Robbins, A. H., & Stout, C. D. (1989). The structure of aconitase. Proteins: Structure, Function, and Bioinformatics, 5(4), 289â312. Portico.

Authors 2

A. H. Robbins (first)
C. D. Stout (additional)

References 59 Referenced 153

10.1038/162963b0
10.1038/164180b0
10.1021/ja01629a073
10.1016/S0021-9258(18)69435-9 / J. Biol. Chem. / Configurational considerations in relation to the mechanisms of the stereospecific enzymatic hydrations of fumarate and cis‐aconitate by Englard S. (1960)
10.1021/ja01478a021
10.1016/S0021-9258(18)96082-5 / J. Biol. Chem. / Mechanism of aconitase action by Rose I. A. (1961)
10.1016/S0021-9258(18)62477-9 / J. Biol. Chem. / The mechanism of aconitase action by Villafranca J. J. (1971)
{'key': 'e_1_2_1_9_2', 'first-page': '229', 'article-title': 'Activation and stabilization of aconitase by ferrous ions', 'volume': '25', 'author': 'Dickman S. R.', 'year': '1950', 'journal-title': 'Arch. Biochem.'} / Arch. Biochem. / Activation and stabilization of aconitase by ferrous ions by Dickman S. R. (1950)
10.1016/0022-2836(68)90403-8
10.1126/science.170.3965.1412
{'key': 'e_1_2_1_12_2', 'first-page': '413', 'volume-title': 'The Enzymes', 'author': 'Glusker J. P.', 'year': '1971'} / The Enzymes by Glusker J. P. (1971)
10.1016/0006-291X(72)90554-2
10.1016/S0021-9258(17)40849-0 / J. Biol. Chem. / The soluble “high potential” type iron‐sulfur protein from mitochondria is aconitase by Ruzicka F. J. (1978)
10.1073/pnas.80.2.393
10.1016/S0021-9258(17)43272-8 / J. Biol. Chem. / Molecular weight of beef heart aconitase and stoichiometry of the components of its iron‐sulfur cluster by Ryden L. (1984)
10.1016/0003-9861(83)90531-3
10.1073/pnas.79.4.1096
10.1016/S0021-9258(17)44390-0 / J. Biol. Chem. / The role of iron in the activation‐inactivation of aconitase by Kennedy M. C. (1983)
10.1016/S0021-9258(17)44391-2 / J. Biol. Chem. / Optical and EPR characterization of different species of active and inactive aconitase by Emptage M. H. (1983)
10.1016/S0021-9258(17)43273-X / J. Biol. Chem. / Incorporation of [35S]sulfide into the Fe‐S cluster of aconitase by Kennedy M. C. (1984)
10.1073/pnas.80.15.4674
{'key': 'e_1_2_1_23_2', 'first-page': '6871', 'article-title': 'Mössbauer studies of aconitase', 'volume': '260', 'author': 'Kent T. A.', 'year': '1985', 'journal-title': 'J. Biol. Chem.'} / J. Biol. Chem. / Mössbauer studies of aconitase by Kent T. A. (1985)
10.1016/S0021-9258(19)89181-0 / J. Biol. Chem. / 17O electron nuclear double resonance characterization of substrate binding to the [4Fe‐4S]1+ cluster of reduced active aconitase by Telser J. (1986)
10.1073/pnas.84.24.8854
10.1021/bk-1988-0372.ch017
10.1021/bi00315a010
10.1021/bi00552a012
10.1021/ja00322a016
10.1021/ja00308a015
10.1016/S0021-9258(18)68459-5 / J. Biol. Chem. / Identification of the reactive sulfhydryl and sequences of cysteinyl‐tryptic peptides from beef heart aconitase by Plank D. W. (1988)
Zalkin H. private communication.
Aul D. andBrown W. E. private communication.
10.1016/S0021-9258(18)89558-8 / J. Biol. Chem. / Iron‐sulfur cluster in aconitase by Robbins A. H. (1985)
10.1073/pnas.86.10.3639
10.1016/S0021-9258(18)34242-X / J. Biol. Chem. / Single crystals of the iron‐sulfur enzyme aconitase by Robbins A. H. (1982)
10.1016/S0021-9258(17)42622-6
10.1107/S0021889885010433
{'key': 'e_1_2_1_39_2', 'first-page': '416', 'volume-title': 'Methods in Enzymology', 'author': 'Hamlin R.', 'year': '1985'} / Methods in Enzymology by Hamlin R. (1985)
10.1016/0076-6879(85)14030-9
10.1107/S0108767383001592
{'key': 'e_1_2_1_42_2', 'first-page': '90', 'volume-title': 'Methods in Enzymology', 'author': 'Wang B. C.', 'year': '1985'} / Methods in Enzymology by Wang B. C. (1985)
10.1016/S0022-2836(68)80010-5
10.1107/S0021889878013308
10.1107/S0365110X60001266
10.1107/S0108767384001471 / Acta Crystallogr. / The use of phase combination in crystallographic refinement: The choice of amplitude coefficients in combined syntehsis by Stuart D. (1985)
10.1107/S0108767388009195
10.1016/S0065-3233(08)60520-3
10.1038/2271098a0
10.1016/S0021-9258(18)33280-0 / J. Biol. Chem. / The presence of a histidine‐aspartic acid pair in the active site of 2‐hydroxyacid dehydrogenases by Birktoft J. J. (1983)
10.1016/0022-2836(87)90191-4
10.1073/pnas.39.6.470
10.1016/0022-2836(82)90452-1
10.1016/S0021-9258(18)68461-3 / J. Biol. Chem. / The state of cluster SH and S2‐ of aconitase during cluster interconversions and removal by Kennedy M. C. (1988)
10.1016/0022-2836(89)90225-8
10.1021/ja00234a038
10.1073/pnas.72.12.4854
10.1016/0005-2795(81)90211-7
10.1016/S0021-9258(18)68460-1 / J. Biol. Chem. / The active site sulfhydryl of aconitase is not required for catalytic activity by Kennedy M. C. (1988)
10.1016/0167-4838(83)90054-7

Dates

Type	When
Created	20 years, 3 months ago (May 28, 2005, 9:02 p.m.)
Deposited	1 year, 10 months ago (Oct. 22, 2023, 3:22 p.m.)
Indexed	3 months ago (May 30, 2025, 12:46 a.m.)
Issued	36 years, 8 months ago (Jan. 1, 1989)
Published	36 years, 8 months ago (Jan. 1, 1989)
Published Online	21 years, 7 months ago (Feb. 3, 2004)
Published Print	36 years, 8 months ago (Jan. 1, 1989)

Funders 0

None

BibTeX

@article{Robbins_1989, title={The structure of aconitase}, volume={5}, ISSN={1097-0134}, url={http://dx.doi.org/10.1002/prot.340050406}, DOI={10.1002/prot.340050406}, number={4}, journal={Proteins: Structure, Function, and Bioinformatics}, publisher={Wiley}, author={Robbins, A. H. and Stout, C. D.}, year={1989}, month=jan, pages={289–312} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        5,
        30
      ]
    ],
    "date-time": "2025-05-30T04:46:14Z",
    "timestamp": 1748580374749
  },
  "reference-count": 59,
  "publisher": "Wiley",
  "issue": "4",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2004,
            2,
            3
          ]
        ],
        "date-time": "2004-02-03T00:00:00Z",
        "timestamp": 1075766400000
      },
      "content-version": "vor",
      "delay-in-days": 5511,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1989,
        1
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>The crystal structure of the 80,000 Da Fe\uf8ffS enzyme aconitase has been solved and refined at 2.1 \u00c5 resolution. The protein contains four domains; the first three from the N\u2010terminus are closely associated around the [3Fe\u20134S] cluster with all three cysteine ligands to the cluster being provided by the third domain. Associationof the larger C\u2010terminal domain with the first three domains createsan extensive cleft leading to the Fe\uf8ffS cluster. Residues from all four domains contribute to the active site region, which is defined by the Fe\uf8ffS cluster and a bound SO<jats:inline-graphic xmlns:xlink=\"http://www.w3.org/1999/xlink\" xlink:href=\"graphic/tex2gif-stack-1.gif\" xlink:title=\"urn:x-wiley:08873585:media:PROT340050406:tex2gif-stack-1\" />ion. This region of the structure contains 4 Arg, 3 His, 3 Ser, 2 Asp, 1 Glu, 3 Asn, and 1 Gln residues, as well asseveral bound water molecules. Three of these side chains reside on a threeturn 3<jats:sub>10</jats:sub> helix in the first domain. The SO<jats:inline-graphic xmlns:xlink=\"http://www.w3.org/1999/xlink\" xlink:href=\"graphic/tex2gif-stack-2.gif\" xlink:title=\"urn:x-wiley:08873585:media:PROT340050406:tex2gif-stack-2\" />ion is bound 9.3 \u00c5 from the center of the [3Fe\u20134S] cluster by the side chains of 2 Arg and 1 Gln rsidues. Each of 3 His side chains in the putative active site is paired with Asp or Glu side chains.</jats:p>",
  "DOI": "10.1002/prot.340050406",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2005,
        5,
        29
      ]
    ],
    "date-time": "2005-05-29T01:02:26Z",
    "timestamp": 1117328546000
  },
  "page": "289-312",
  "source": "Crossref",
  "is-referenced-by-count": 153,
  "title": "The structure of aconitase",
  "prefix": "10.1002",
  "volume": "5",
  "author": [
    {
      "given": "A. H.",
      "family": "Robbins",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "C. D.",
      "family": "Stout",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2004,
        2,
        3
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_1_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/162963b0"
    },
    {
      "key": "e_1_2_1_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/164180b0"
    },
    {
      "key": "e_1_2_1_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/ja01629a073"
    },
    {
      "key": "e_1_2_1_5_2",
      "doi-asserted-by": "crossref",
      "first-page": "1510",
      "DOI": "10.1016/S0021-9258(18)69435-9",
      "article-title": "Configurational considerations in relation to the mechanisms of the stereospecific enzymatic hydrations of fumarate and cis\u2010aconitate",
      "volume": "235",
      "author": "Englard S.",
      "year": "1960",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/ja01478a021"
    },
    {
      "key": "e_1_2_1_7_2",
      "doi-asserted-by": "crossref",
      "first-page": "1870",
      "DOI": "10.1016/S0021-9258(18)96082-5",
      "article-title": "Mechanism of aconitase action",
      "volume": "242",
      "author": "Rose I. A.",
      "year": "1961",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_8_2",
      "doi-asserted-by": "crossref",
      "first-page": "772",
      "DOI": "10.1016/S0021-9258(18)62477-9",
      "article-title": "The mechanism of aconitase action",
      "volume": "246",
      "author": "Villafranca J. J.",
      "year": "1971",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_9_2",
      "first-page": "229",
      "article-title": "Activation and stabilization of aconitase by ferrous ions",
      "volume": "25",
      "author": "Dickman S. R.",
      "year": "1950",
      "journal-title": "Arch. Biochem."
    },
    {
      "key": "e_1_2_1_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(68)90403-8"
    },
    {
      "key": "e_1_2_1_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.170.3965.1412"
    },
    {
      "key": "e_1_2_1_12_2",
      "first-page": "413",
      "volume-title": "The Enzymes",
      "author": "Glusker J. P.",
      "year": "1971"
    },
    {
      "key": "e_1_2_1_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-291X(72)90554-2"
    },
    {
      "key": "e_1_2_1_14_2",
      "doi-asserted-by": "crossref",
      "first-page": "2514",
      "DOI": "10.1016/S0021-9258(17)40849-0",
      "article-title": "The soluble \u201chigh potential\u201d type iron\u2010sulfur protein from mitochondria is aconitase",
      "volume": "253",
      "author": "Ruzicka F. J.",
      "year": "1978",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.80.2.393"
    },
    {
      "key": "e_1_2_1_16_2",
      "doi-asserted-by": "crossref",
      "first-page": "3141",
      "DOI": "10.1016/S0021-9258(17)43272-8",
      "article-title": "Molecular weight of beef heart aconitase and stoichiometry of the components of its iron\u2010sulfur cluster",
      "volume": "259",
      "author": "Ryden L.",
      "year": "1984",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-9861(83)90531-3"
    },
    {
      "key": "e_1_2_1_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.79.4.1096"
    },
    {
      "key": "e_1_2_1_19_2",
      "doi-asserted-by": "crossref",
      "first-page": "11098",
      "DOI": "10.1016/S0021-9258(17)44390-0",
      "article-title": "The role of iron in the activation\u2010inactivation of aconitase",
      "volume": "258",
      "author": "Kennedy M. C.",
      "year": "1983",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_20_2",
      "doi-asserted-by": "crossref",
      "first-page": "11106",
      "DOI": "10.1016/S0021-9258(17)44391-2",
      "article-title": "Optical and EPR characterization of different species of active and inactive aconitase",
      "volume": "258",
      "author": "Emptage M. H.",
      "year": "1983",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_21_2",
      "doi-asserted-by": "crossref",
      "first-page": "3145",
      "DOI": "10.1016/S0021-9258(17)43273-X",
      "article-title": "Incorporation of [35S]sulfide into the Fe\u2010S cluster of aconitase",
      "volume": "259",
      "author": "Kennedy M. C.",
      "year": "1984",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.80.15.4674"
    },
    {
      "key": "e_1_2_1_23_2",
      "first-page": "6871",
      "article-title": "M\u00f6ssbauer studies of aconitase",
      "volume": "260",
      "author": "Kent T. A.",
      "year": "1985",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_24_2",
      "doi-asserted-by": "crossref",
      "first-page": "4840",
      "DOI": "10.1016/S0021-9258(19)89181-0",
      "article-title": "17O electron nuclear double resonance characterization of substrate binding to the [4Fe\u20104S]1+ cluster of reduced active aconitase",
      "volume": "261",
      "author": "Telser J.",
      "year": "1986",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.84.24.8854"
    },
    {
      "key": "e_1_2_1_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bk-1988-0372.ch017"
    },
    {
      "key": "e_1_2_1_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00315a010"
    },
    {
      "key": "e_1_2_1_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00552a012"
    },
    {
      "key": "e_1_2_1_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/ja00322a016"
    },
    {
      "key": "e_1_2_1_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/ja00308a015"
    },
    {
      "key": "e_1_2_1_31_2",
      "doi-asserted-by": "crossref",
      "first-page": "8184",
      "DOI": "10.1016/S0021-9258(18)68459-5",
      "article-title": "Identification of the reactive sulfhydryl and sequences of cysteinyl\u2010tryptic peptides from beef heart aconitase",
      "volume": "263",
      "author": "Plank D. W.",
      "year": "1988",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_32_2",
      "unstructured": "Zalkin H. private communication."
    },
    {
      "key": "e_1_2_1_33_2",
      "unstructured": "Aul D. andBrown W. E. private communication."
    },
    {
      "key": "e_1_2_1_34_2",
      "doi-asserted-by": "crossref",
      "first-page": "2328",
      "DOI": "10.1016/S0021-9258(18)89558-8",
      "article-title": "Iron\u2010sulfur cluster in aconitase",
      "volume": "260",
      "author": "Robbins A. H.",
      "year": "1985",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.10.3639"
    },
    {
      "key": "e_1_2_1_36_2",
      "doi-asserted-by": "crossref",
      "first-page": "9061",
      "DOI": "10.1016/S0021-9258(18)34242-X",
      "article-title": "Single crystals of the iron\u2010sulfur enzyme aconitase",
      "volume": "257",
      "author": "Robbins A. H.",
      "year": "1982",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(17)42622-6"
    },
    {
      "key": "e_1_2_1_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1107/S0021889885010433"
    },
    {
      "key": "e_1_2_1_39_2",
      "first-page": "416",
      "volume-title": "Methods in Enzymology",
      "author": "Hamlin R.",
      "year": "1985"
    },
    {
      "key": "e_1_2_1_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0076-6879(85)14030-9"
    },
    {
      "key": "e_1_2_1_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1107/S0108767383001592"
    },
    {
      "key": "e_1_2_1_42_2",
      "first-page": "90",
      "volume-title": "Methods in Enzymology",
      "author": "Wang B. C.",
      "year": "1985"
    },
    {
      "key": "e_1_2_1_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0022-2836(68)80010-5"
    },
    {
      "key": "e_1_2_1_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1107/S0021889878013308"
    },
    {
      "key": "e_1_2_1_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1107/S0365110X60001266"
    },
    {
      "key": "e_1_2_1_46_2",
      "doi-asserted-by": "crossref",
      "first-page": "713",
      "DOI": "10.1107/S0108767384001471",
      "article-title": "The use of phase combination in crystallographic refinement: The choice of amplitude coefficients in combined syntehsis",
      "volume": "40",
      "author": "Stuart D.",
      "year": "1985",
      "journal-title": "Acta Crystallogr."
    },
    {
      "key": "e_1_2_1_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1107/S0108767388009195"
    },
    {
      "key": "e_1_2_1_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0065-3233(08)60520-3"
    },
    {
      "key": "e_1_2_1_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/2271098a0"
    },
    {
      "key": "e_1_2_1_50_2",
      "doi-asserted-by": "crossref",
      "first-page": "472",
      "DOI": "10.1016/S0021-9258(18)33280-0",
      "article-title": "The presence of a histidine\u2010aspartic acid pair in the active site of 2\u2010hydroxyacid dehydrogenases",
      "volume": "258",
      "author": "Birktoft J. J.",
      "year": "1983",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(87)90191-4"
    },
    {
      "key": "e_1_2_1_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.39.6.470"
    },
    {
      "key": "e_1_2_1_53_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(82)90452-1"
    },
    {
      "key": "e_1_2_1_54_2",
      "doi-asserted-by": "crossref",
      "first-page": "8194",
      "DOI": "10.1016/S0021-9258(18)68461-3",
      "article-title": "The state of cluster SH and S2\u2010 of aconitase during cluster interconversions and removal",
      "volume": "263",
      "author": "Kennedy M. C.",
      "year": "1988",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_55_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(89)90225-8"
    },
    {
      "key": "e_1_2_1_56_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/ja00234a038"
    },
    {
      "key": "e_1_2_1_57_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.72.12.4854"
    },
    {
      "key": "e_1_2_1_58_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0005-2795(81)90211-7"
    },
    {
      "key": "e_1_2_1_59_2",
      "doi-asserted-by": "crossref",
      "first-page": "8190",
      "DOI": "10.1016/S0021-9258(18)68460-1",
      "article-title": "The active site sulfhydryl of aconitase is not required for catalytic activity",
      "volume": "263",
      "author": "Kennedy M. C.",
      "year": "1988",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_60_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0167-4838(83)90054-7"
    }
  ],
  "container-title": "Proteins: Structure, Function, and Bioinformatics",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1002%2Fprot.340050406",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1002/prot.340050406",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        10,
        22
      ]
    ],
    "date-time": "2023-10-22T19:22:09Z",
    "timestamp": 1698002529000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1002/prot.340050406"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1989,
        1
      ]
    ]
  },
  "references-count": 59,
  "journal-issue": {
    "issue": "4",
    "published-print": {
      "date-parts": [
        [
          1989,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1002/prot.340050406"
  ],
  "URL": "http://dx.doi.org/10.1002/prot.340050406",
  "relation": {},
  "ISSN": [
    "0887-3585",
    "1097-0134"
  ],
  "subject": [],
  "container-title-short": "Proteins",
  "published": {
    "date-parts": [
      [
        1989,
        1
      ]
    ]
  }
}